Fibrillar collagens are a metazoan innovation that are a part of the extracellular matrix of muscle, skeleton, and other connective tissues. Comprised of three families of genes (Clade A, Clade B, Clade C), they underwent duplication and neofunctionalization in the jawed vertebrate lineage (gnathostomes). Previous work has suggested that ancestral chordates possessed only four fibrillar collagens (2A’s, 1B, 1C) while most jawed vertebrates have eleven (5A’s, 4B’s, 2C’s). The evolution of vertebrates from invertebrate chordates also coincided with morphological novelties, so we asked whether the duplication of fibrillar collagens was linked to the origin of these novel cell types. We used the jawless lamprey Petromyzon marinus to test this question, as they diverged from gnathostomes more than 500 million years ago and could thus provide insight into the stepwise evolutionary process in vertebrates. We discovered twelve fibrillar collagens in lamprey (6A’s, 5B’s, 1C) and were able to identify several lineage-specific duplications. Between lamprey and gnathostome orthologs, we found that lamprey collagens were less specific in the musculoskeletal system, being coexpressed more often in both muscle and skeleton. However, we found that some lamprey paralogs were subfunctionalized in lamprey-specific morphology like mucocartilage as well as the epi/hypobranchial musculature. Our results suggest that the last common ancestor of gnathostomes and lamprey had seven fibrillar collagens (3A’s, 2B’s, 2C’s) with redundant expression across the musculoskeletal system. We also posit that some innovations to the gnathostome and lamprey muscle and skeleton may have been the result of collagen duplication and subfunctionalization.